Effects of incubation temperature on hatchling phenotypes in an oviparous lizard with prolonged egg retention: are the two main hypotheses on the evolution of viviparity compatible?

Rodríguez-Díaz, Tania; González, Francisco; Ji, Xiang; Braña, F.

doi:10.1016/j.zool.2009.05.001

Cited by 32 publications

(35 citation statements)

References 31 publications

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“…We performed all trials overnight (approximately 19:00-08:00 h) in a dark climatic chamber (brand Liebherr, Dortmund, Germany), because it was previously shown that Z. vivipara stop all activity when placed in the dark (Cragg, 1978). All trials were carried out at 30±0.5°C, which broadly corresponds to the preferred body temperature of reproductive females (LeGalliard et al, 2003;Rodríguez-Díaz et al, 2010). Lizards were placed individually into test containers (1000 ml) within the chamber and were allowed to acclimatize for 1 h before beginning a trial.…”

Section: Oxygen Consumptionmentioning

confidence: 99%

Influence of reproductive mode on metabolic costs of reproduction: insight from the bimodal lizard Zootoca vivipara

Foucart

Lourdais

DeNardo

et al. 2014

Journal of Experimental Biology

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Examination of the selective forces behind the transition from oviparity to viviparity in vertebrates must include an understanding of the relative energy costs of the two reproductive modes. However, interspecific comparisons of reproductive mode are confounded by numerous other inherent differences among the species. Therefore, we compared oxygen consumption, as a reflection of energy costs, during reproduction in oviparous and viviparous females of the reproductively bimodal lizard Zootoca vivipara (Jaquin 1787). Female oxygen consumption progressively increased over the course of reproduction, peaking just prior to parition when it was 46% (oviparous form) and 82% (viviparous form) higher than it was at the pre-reproductive stage. Total increase in oxygen consumption (TIOC) during the pre-ovulation period was not different between the reproductive modes. Conversely, post-ovulation TIOC was more than three times higher in viviparous females, reflecting a dramatic increase in embryonic metabolism as well as maternal metabolic costs of pregnancy (MCP). MCP accounted for 22% of total metabolism in viviparous females, whereas it was negligible in oviparous females. Our results demonstrate that egg retention through the first third of development, as is typical of most oviparous squamates, entails minimal maternal energy demand, while extending retention imposes much greater metabolic constraints. Selection for transition from oviparity to viviparity must therefore provide benefits that outweigh not only the added burden associated with prolonged embryonic retention, but also the substantial additional energy costs that are incurred.

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Section: Oxygen Consumptionmentioning

confidence: 99%

Influence of reproductive mode on metabolic costs of reproduction: insight from the bimodal lizard Zootoca vivipara

Foucart

Lourdais

DeNardo

et al. 2014

Journal of Experimental Biology

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show abstract

“…Female Z. vivipara prefer a lower body temperature during pregnancy (mean body temperature ± SD: 32.33 ± 1.27°C; n = 64) than do adult males or non pregnant adult females (34.05 ± 1.07°C; n = 155; data from this population: Rodríguez-Díaz et al 2010). If pregnant females prefer lower body temperatures to optimize embryonic development, even at the cost of some increase in incubation time, then incubating eggs in utero at the higher temperatures preferred by non-gravid females can be expected to have some detrimental effects on embryogenesis, and thus on hatchling phenotypes.…”

Section: Methodsmentioning

confidence: 91%

“…Chalcides ocellatus: Daut and Andrews 1993; Hoplodactylus maculatus: Rock et al 2000), and this increase in body temperature would accelerate embryonic development inside the mother's body (Mathies and Andrews 1997;Shine 2006). Shift in thermal preferendum during pregnancy, especially toward lower body temperatures that retard development (but see Rodríguez-Díaz et al 2010), is assumed to be related to optimising the conditions for embryogenesis (Beuchat 1988;Mathies and Andrews 1997;Rodríguez-Díaz et al 2010) and could favour the evolution of extended egg retention since a longer intrauterine stay would extend the time of the developing embryos' exposure to suitable conditions (Braña and Ji 2007).…”

Section: Introductionmentioning

confidence: 99%

“…To test this prediction, we evaluated the role of gestation environment on embryonic development, hatching success, and hatchling phenotype in oviparous Zootoca vivipara (Jacquin 1797), by keeping a group of gravid females at a higher temperature than they would normally select, i.e. similar to that preferred by non-gravid females of the same population, as determined in a laboratory thermal gradient (Rodríguez-Díaz et al 2010). We chose this experimental approach rather than a possible alternative consisting of inducing oviposition (see Mathies and Andrews 1995) and then incubating the eggs under the selected thermal regime because our model more closely resembles the natural conditions of the incubation environment inside the mother's oviduct with the exception of the thermal regime applied.…”

Section: Introductionmentioning

confidence: 99%

“…We chose this experimental approach rather than a possible alternative consisting of inducing oviposition (see Mathies and Andrews 1995) and then incubating the eggs under the selected thermal regime because our model more closely resembles the natural conditions of the incubation environment inside the mother's oviduct with the exception of the thermal regime applied. Our study organism is an ideal model for this task not only because females shift their preferred temperature during pregnancy, but also because they lay eggs with the embryo at quite an advanced stage of development (31-34 according to Dufaure and Hubert's 1961 developmental table;Braña et al 1991, Rodríguez-Díaz et al 2010. The species Z. vivipara also includes viviparous populations that lay soft-shelled eggs with fully developed hatchlings that emerge a few hours after oviposition (Panigel 1956).…”

Section: Introductionmentioning

confidence: 99%

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Shift in Thermal Preferences of Female Oviparous Common Lizards During Egg Retention: Insights into the Evolution of Reptilian Viviparity

Rodríguez-Díaz

Braña

2011

Evol Biol

Self Cite

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Pregnant female Zootoca vivipara select lower body temperatures than males or nonpregnant females, and this shift in the thermal preferendum is believed to be related to optimising the conditions for embryogenesis. Thus, subjecting embryos to the higher temperature selected by males and non-gravid females might have detrimental effects on embryonic development and on hatchling fitness, according to predictions of the ''maternal manipulation'' hypothesis on the evolution of viviparity. To test the role of gestation environment on embryonic development in oviparous Z. vivipara, we kept a number of gravid females at the temperature selected by non-gravid females in a laboratory thermal gradient, whereas control females were allowed to regulate their body temperature without restrictions. Developmental stage at oviposition was more advanced for embryos of the experimental clutches, which were heavier than those of the control group. Forced gestation temperature also affected hatching success (58.62% in the experimental treatment vs. 97.37% in the control group). In addition, hatchlings from females subjected to high temperatures during pregnancy were smaller, had shorter head length and performed worse in running trials. Our results fulfil the prediction of the ''maternal manipulation'' hypothesis, and suggest that the shift in female body temperature during pregnancy optimizes embryogenesis and hatchling phenotype by avoiding the negative effects of the high incubation temperatures preferred by non-gravid females.

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Influence of size, sex, and reproductive status on the thermal biology of endemic Florida scrub lizards

Gainsbury

2020

Ecology and Evolution

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Climate change is impacting species globally, with many populations declining at an accelerated rate toward extinction. Ectothermic species are particularly vulnerable given their reproductive success is linked to environmental temperatures. Studies of the effect of temperature on reproductive success in oviparous squamates have focused mostly on nest temperatures, after eggs are deposited. However, in some species gravid females are known to thermoregulate differently than other adults to increase reproductive success. It is essential to understand what influences the thermal biology of breeding adults in a population to implement targeted conservation strategies. The Florida scrub lizard Sceloporus woodi is an endemic species listed as near-threatened due to decreasing populations. This study is the first to document the thermal biology of these breeding adults in relation to size, sex, and reproductive status. A t test was used to determine whether sexual dimorphism was present in the sampled S. woodi. Full linear mixed-effects models were used to test the influence of size, sex, and reproductive status on the thermal biology of S. woodi. Despite femalebiased sexual size dimorphism, there were no sex-based differences in body temperature in the studied population. Interestingly, reproductive status influenced thermal biology of females during the breeding season, with gravid females maintaining lower body temperatures compared to nongravid females. However, gravid females did not regulate their body temperatures more precisely compared to nongravid females. These results indicate the population viability of this endemic species is potentially linked to the different thermoregulatory requirements of gravid females as compared to other adults. Lower body temperatures of gravid females, exacerbated by their lack of thermal precision, have disconcerting conservation implications in the face of climate warming. Future studies focusing on gravid females are warranted to attain effective biodiversity conservation strategies mitigating the impacts of climate warming.

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Effects of incubation temperature on hatchling phenotypes in an oviparous lizard with prolonged egg retention: are the two main hypotheses on the evolution of viviparity compatible?

Cited by 32 publications

References 31 publications

Influence of reproductive mode on metabolic costs of reproduction: insight from the bimodal lizard Zootoca vivipara

Influence of reproductive mode on metabolic costs of reproduction: insight from the bimodal lizard Zootoca vivipara

Shift in Thermal Preferences of Female Oviparous Common Lizards During Egg Retention: Insights into the Evolution of Reptilian Viviparity

Influence of size, sex, and reproductive status on the thermal biology of endemic Florida scrub lizards

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